bivalves with 'concrete overcoats': granicorium and samarangia

Bivalves with `concrete overcoats': Granicorium andSamarangiaJ. D. Taylor1, E.A. Glover1 and C. J. R. Braithwaite2

1Department of Zoology,The Natural History Museum,London SW7 5BD, UK2Division of Earth Sciences,The University of Glasgow,

Glasgow G12 8QQ, UK

Keywords:

bivalves, avenaceous layers, cement,shell formation

Accepted for publication:14 January 1999

AbstractTaylor, J. D. Glover, E. A. and Braithwaite, C. J. R. 1999. Bivalves with`concrete overcoats': Granicorium and Samarangia. Ð Acta Zoologica(Stockholm) 80: 285±300

Two veneroidean bivalves Granicorium indutum from Australia andSamarangia quadrangularis from the tropical Indo-Pacific region, cement athick, hard layer of sand over most of their shells. In Granicorium this layerforms low commarginal ribs while in Samarangia it forms more prominentradial features. Sand grains are cemented to the shell and to each other withgrowths of a crystalline aragonitic cement similar in morphology toinorganic marine cements. Both species secrete mucus layers at the growingshell margin which initially hold the sediment grains together and form asubstrate for the nucleation and growth of calcium carbonate crystals. Theribs of Samarangia are formed by the accretion of successive sheets ofspherulitic growths. In G. indutum, the middle and outermost of two innermantle folds are large, glandular and capable of considerable extensionbeyond the shell margin. Mucus secreted by the folds contains abundantbacteria and small calcium carbonate crystals. It is proposed that initialnucleation of the calcium carbonate cement takes place within this biofilmpossibly mediated by the bacteria. The function of the sand layers isunknown but predation resistance and protection of the shells fromendobionts are the most likely possibilities.

John Taylor, Department of Zoology, The Natural History Museum, LondonSW7 5BD, UK. E-mail: [email protected]

Introduction

The shells of bivalve molluscs have received muchattention in terms of the description and functionalanalysis of shape, microstructure, hinge structure andexternal ornament (Taylor et al. 1969, 1973; Stanley 1970,1975; Vermeij 1978, 1987; Savazzi 1982; Seilacher 1985;Carter 1990). However, it is being increasingly recognizedthat bivalves also secrete or form a large variety of othermineralized and nonmineralized structures which, whileextraneous to the main shell layers should, nevertheless, beconsidered as part of it in functional terms. These includeelaborations of the periostracum into flanges and hairs(Bottjer and Carter 1980; Harper 1997a), calcareousspicules, spines and granules embedded in the periostra-cum (Aller 1974; Carter and Aller 1975; Carter 1990),

calcareous encrustations of various types (Carter 1990;Morton 1993; Ohno 1996) and sediment coatings on theperiostracum (Prezant 1981a). Additionally, there arecalcified tubes, crypts and encasings of various forms(Savazzi 1982; Morton 1983, 1984, 1985, 1993, 1995).Although these structures are extremely diverse, incomparison with the primary shell little is known of theirformation or function. The study of these extra-and intra-periostracal encrustations and calcification is hampered bythe fact that in museum collectons shells have often beencarefully cleaned (as is the case of the holotype ofSamarangia quadrangularis (Adams & Reeve, 1850) in themistaken belief that the coatings are inorganic andextraneous to the animal.

During a survey of subtidal marine molluscs fromaround Rottnest Island, near Fremantle, Western Australia

q 1999 The Royal Swedish Academy of Sciences 285

Acta Zoologica (Stockholm) 80: 285±300 (October 1999)

we dredged a few specimens of an unusual bivalvemollusc, Granicorium indutum Hedley 1906 (Veneroidea,currently subfamily Tapetinae). This subspherical bivalveis remarkable because the shell is encrusted with a thick,hard coating of sandy sediment which is as thick, orthicker, than the calcified shell itself. This is not asecondary, inorganic encrustation, but a primary construcË-tional feature. The only other bivalve known to us with athick cemented arenaceous layer comparable to that ofGranicorium is another veneroidean, Samarangia quadran-gularis (Adams & Reeve 1850), currently placed in themonospecific subfamily Samaranginae (Keen 1969). Thisanimal has the additional feature that the arenaceous layeris formed into rough radial ribs (Clench 1942; Loch1989). Both Granicorium and Samarangia are rare inmuseum collections, their biology is entirely unknown andtheir relationships are uncertain. Apart from the originaldescription of the genus and species from MastheadIsland, central Queensland (Hedley 1906), Granicoriumhas received only passing reference in the literature (Slack-Smith 1990; Lamprell and Whitehead 1992).

It is important to differentiate arenaceous layers, whichare formed by the animal at the same time as the shell,from secondary inorganic deposition such as manganeseoxide encrustations which often occur on the shells ofsubtidal molluscs from muddy habitats and form withoutdirect action from the animal (Allen 1960). Arenaceouslayers should also be distinguished from the extra-and in-traperiostracal calcification seen in some bivalves (Litho-phaginae and Veneridae) which is often in the form ofspines and needles that without magnification can appearas an encrustation on the shell surface (Carter 1990; Ohno1996). Thin and fragile arenaceous coatings are knownfrom some anomalodesmatan bivalves such as Lyonsia andEntodesma in the family Lyonsidae (Prezant 1981a; Harper1997a; fig. 4D), and some species of the veneroideansubfamily Pitarinae also apparently have thin sedimentcoatings (e.g. Oliver 1995; p. 270 Pitar yerburi, P. tumida)but these features have never been studied. A number ofother bivalves, such as Cooperella subdiaphana (Carpenter)(Petricolidae) secrete arenaceous `nests' and crypts whichdo not adhere to the shell (Morton 1995).

The objectives of this paper are to determine themechanism by which Granicorium and Samarangia encrusttheir shells with sand and to consider the possiblefunctions of this arenaceous layer.

Materials and Methods

Specimens of Granicorium were collected by dredge fromaround Rottnest Island, off Fremantle, Western Australia(details in Glover and Taylor 1999, in press). All materialof Granicorium indutum collected, including thin sections,is housed in the collections of the Department of Zoology,The Natural History Museum, London. Other material,

including the type specimens of G. indutum and G.attonitum Iredale (1936); was examined from thecollections of the Australian Museum, Sydney, and theMuseum and Art Gallery of the Northern Territory,Darwin. Specimens of Samarangia quadrangularis werestudied from the collections of the MuseÂum Nationald'Histoire Naturelle, Paris. At least two individuals hadbeen live-collected but no preserved animals wereavailable. The holotype of S. quadrangularis was alsoexamined (NHM London).

After collection, individuals of Granicorium indutum wererelaxed using a few drops of propylene phenoxetol inseawater and then preserved in 80% ethanol. Histologicalsections were made of pieces of the mantle edge cut at8 mm and stained in Mallory's triple and haemalum/eosin.Pieces of the mantle margin were sliced with a razor bladeand taken through ascending concentrations of acetoneand then critical point dried using liquid CO2. These werecoated with Au/Pd alloy and examined by scanningelectron microscopy (SEM).

The microstructure of the true shell was studied usingacetate peels made from cut, polished and etched sectionsof the shell. The arenaceous layers of Granicorium andSamarangia were investigated by geological thin sections ofthe shell which had been embedded in resin blocks. Thearenaceous layers and shell margins were also examined bySEM of cut and fractured pieces of the shell.

The cement was investigated using plain polarized light,UV fluorescence, and cathode luminescence. Themineralogy was determined on the basis of crystalmorphology, EDX-analysis, and trace element mapping byelectron microprobe.

Results

General features of Granicorium indutum and Samarangiaquadrangularis

Granicorium indutum is a subspherical (Fig. 1A-C, G),globose bivalve with a maximum length of about 40±50 mm and almost entirely covered with the thick,cemented arenaceous layer. The outer surface of the sandlayer is generally smooth except for low, rounded,concentric undulations (Fig. 1A). The underlying shell isglossy, with very fine growth lines. All the shell is coveredby the sand layer except for a tiny area of 1±2 mm at thetip of the umbones (Fig. 1B). In live-collected animalsthere is no encrusting epibiota or boring endobiota ineither the sand layer or shell.

Samarangia quadrangularis (Fig. 1D-F,H) is subquadrateto subcircular in outline with a maximum height of about60±70 mm. The shell is almost completely encrusted witha thick cemented sand layer which has up to 10 radialridges extending from the umbone to the ventral margin.The ridges may be broader and more flared on the

286 q The Royal Swedish Academy of Sciences

Sand-accreting bivalves . Taylor, Glover and Braithwaite Acta Zoologica (Stockholm) 80: 285±300 (October 1999)

posterior of the shell (Fig. 1D,E). As in Granicorium thetrue shell surface is glossy and smooth with fine growthlines and the shell itself relatively thin. The tips of theumbones are again free of sand. Samarangia differs fromGranicorium in its larger size, less inflated shell and theradial ridges in the arenaceous layer.

The shell microstructures of G. indutum and S. quadran-gularis are similar and comprise an outer crossed-lamellarlayer, a middle homogeneous layer and an inner layer,within the pallial line, consisting of homogeneousstructure, with small patches of complex crossed-lamellarstructure beneath the hinge (Group III type as classified by

Fig. 1ÐA-C, Granicorium indutum, Rottnest Island, WesternAustralia. ÐA, exterior of right valve. ÐB, dorsal view. ÐC,interior of right valve. ÐD-F, Samarangia quadrangularis. ÐD,exterior of right valve. New Caledonia 218490S 1668380E, 50 m(MNHN, Paris). ÐE, exterior of right valve. Chesterfield Bank,

`Coriolis' station DW125, 198280S 158240E, 54 m (MNHN,Paris). ÐF, interior of right valve. Note drill hole made bypredatory gastropod. ReÂunion, 75 m (MNHN, Paris). ÐG, G.indutum, hinge of right valve. ÐH, S. quadrangularis, hinge ofright valve (details as F.). Scale bars: 5 mm.


Acta Zoologica (Stockholm) 80: 285±300 (October 1999) Taylor, Glover and Braithwaite . Sand-accreting bivalves

Shimamoto 1986). The first-order lamellae of the outerlayer have a sigmoidal alignment (type C of Shimamoto1986 fig. 9c). Both Granicorium and Samarangia have athin periostracum of around 2±3 mm

Anatomy

The focus of this study is the formation of the arenaceouslayer and only the main anatomical features of G. indutum,apart from the mantle edge, are outlined here (Fig. 2). Nopreserved animals of Samarangia were available.

The ctenidia of G. indutum are large with the outerdemibranch smaller than the inner. The labial palps arelarge with 7±8 folds on the inner margin. The foot is ofmedium size and pointed at the anterior end. Exceptaround the siphonal area, the mantle is unfused with alarge pedal gape extending from the anterior adductormuscle to just ventral of the inhalant aperture. Theinhalant and exhalant apertures are formed from fusion ofthe inner mantle fold only. The inhalant and exhalantsiphons are very short and fringed with papillae.

The mantle margin is unusual in having a very smallouter mantle fold (Fig. 3A) and periostracal groove. Thelatter is deep and lined with a thin layer of cuboidal cells.

Fig. 2ÐGranicorium indutum, general anatomy, left mantleremoved. aa, anterior adductor muscle; exa, exhalant aperture;f, foot; id, inner demibranch; imf; inner mantle fold; ina,inhalant aperture; k, kidney; lp, labial palp; od, outerdemibranch; omf, middle and outer mantle folds; pa, posterioradductor muscle.

Fig. 3ÐGranicorium indutum, radial section through the mantlemargin. ÐA, section from the line of pallial attachment to themantle margin. Scale bar: 200 mm. ÐB, detail of middle andouter folds. crt, ciliated rejection tract; gc, gland cells; imf (1),

inner mantle fold 1; imf (2), inner mantle fold 2; mmf, middlemantle fold; omf, outer mantle fold; p, periostracum; pg,periostracal groove; pl, muscle attachment at pallial line; pn,pallial nerve.



The middle fold is large and muscular with subepithelialgland cells on the outermost margin; some preparationsshow this middle fold divided into two lobes (Fig. 3A).There are two inner mantle folds (the homology of thesefolds is uncertain and the naming is arbitrary), theoutermost of these (imf1) is highly enlarged and forms afluted ridge around the inside of the mantle edge (Fig. 2,3B). The outer face of the ridge tapers to a sharp edge.The whole of this fold is highly muscular, with sets oftransverse and radial muscles. Additionally, there areabundant subepithelial gland cells on the outer and upperfaces (Fig. 3A). The second of two inner folds (imf2) issmaller and forms a low rounded ridge. This fold containsnerve endings and sensory cells. From this fold to thepallial line the inner mantle epithelium is ciliated (ciliatedrejection tract). Our SEM preparations show that both themiddle and inner fold 1 are subject to considerable shapechanges and with their extensive musculature are probablyhighly mobile in life and capable of being extended beyondthe shell margin.

Habitat and distribution

Seven live individuals of Granicorium indutum from a totalof 1685 living bivalves were found on the narrow, swell-dominated, open shelf (Collins 1988) around RottnestIsland. They lived at depths of between 26 and 38 m inwell-sorted, coarse, quartz-rich sand. The associatedmolluscan fauna comprised predominantly the bivalvesGlycymeris striatularis and G. persimilis with other speciesincluding Eucrassatella donacina, Megacardita rubicundumand Barbatia foliata. More widely, the distribution ofGranicorium ranges from central Queensland (SwainsReef) to Shark Bay, Western Australia, including the GreatAustralian Bight, although we found no records fromVictoria and South Australia (museum records and Slack-Smith 1990). Records indicate that Granicorium lives atdepths of between 30 and 150 m in sandy substrates.

Little information is available for Samarangia quadrangu-laris. Museum and literature records show that it is knownfrom Okinawa, the Philippines, eastern Indonesia, centralQueensland, New Caledonia, Vanuatu, ReÂunion and theRed Sea (Oliver 1992). It lives in shallow water from 3 to70 m, often in sand patches adjacent to coral reefs or onhard substrates (Loch 1989). Unlike Granicorium,Samarangia is entirely tropical in distribution.

Structure of the arenaceous layer

The most remarkable feature of the shells of Granicoriumand Samarangia is the presence of the thick layer of hardsand adhering to the outside of the shell (Fig. 1A,B,D,E)and we describe the structure of this in some detail.

a. Granicorium. In Granicorium, this layer consists ofmainly quartz grains and biogenic carbonate grains (mean

0.32 � sd 0.13 mm, max. 0.63, min. 0.08 (n = 58), heldtogether by a calcareous cement. On the median tomarginal parts of the sectioned shell the sand layer is 1.2±1.5 times thicker than the shell. Towards the umbonal areathe shell is about twice as thick as the arenaceous layer,but this is where inner shell layer is being actively formed.The outer surface of the sand layer is generally smoothexcept for low, rounded, concentric undulations (Fig. 1A).

In thin section, the sand grains are arranged with theirlong axes inclined away from the margin (Fig. 4A). Themineral cement binding them consists of closely packedelongate crystals with their long axes at right angles to thesubstrate (Fig. 4B). There is a marked asymmetry in thedistribution of this cement; growths of the cement are sig-nificantly thicker on grain surfaces facing towards the shellmargin, while those facing away carry little or no cement.Typical cement thicknesses are 20±40 mm. In a few areasthe cement surface is strongly convex forming smoothlyrounded botryoids. Locally the cement is multilaminarsuggesting several phases of growth, but laminae taperlaterally and some are discontinuous. Electron microprobeelement mapping indicates that the cement containsrelatively large quantities of strontium but little or nomagnesium, suggesting that the crystals are aragonite.

Scanning microscopy of the cement shows siliciclasticgrains carry growths of elongate (acicular) crystals, someof which are roughly rectangular in section (resemblingmarine aragonite cement, e.g. Schroeder 1972). Theseoccur in open radiating clusters (Fig. 4D) and in spherularbundles of closely aligned crystals that form dense masseswith smooth rounded outer surfaces (Fig. 4C). Successivegrowth stages are marked by concentric layers. Theaccreting surface at the shell margin shows quartz andbiogenic grains encrusted with granular crystals (around1±2 mm) but also areas where the sediment grains arecoated with `mucus' sheets with crystals growing bothwithin and beneath the sheets (Fig. 4E,F). These crystalsare up to 5±8 mm long with ends tapering to a rice-grainform.

b. Samarangia. As in Granicorium, the agglutinatedsediment grains are arranged with their long axes inclinedaway from the margin and held together by an aragoniticcement consisting of fibrous crystals with their long axesaligned normal to the substrate. The cement varies inthickness but is markedly asymmetrical, with thickergrowths facing towards the shell margin. Along the outershell surface the cement growths commonly form L-shaped accumulations in the angles between the shell andoverlying grains (Fig. 5A-B), tapering upwards (away fromthe shell) and forwards along the shell surface towards themargin. In some areas crystals are crossed by growth linesreflecting successive stages of growth of the cement.Locally however, these converge so that particular layersthin rapidly. At some distance from the margin smallamounts of calcite cement are developed on some forami-



niferal surfaces and small amounts of `typical' marinecement are present within some pores enclosed withinskeletal fragments (Fig. 5G) but these are not widespread.

The distinctive feature of Samarangia is the formation ofthe `ribs' in the arenaceous layer (Fig. 1D,E). Sectionsshow that these are formed by successions of crystallinesheets that are inclined away from the shell margin.(Fig. 5A,C). The larger of these sheets are produced byfusion and extension of successive smaller sheets. Inter-mediary sheets elevate only a short distance above the shellsurface before thinning out (Fig. 5B,C) The cement sheetsare around 20±50 mm thick and composed of radialbundles (spherulites) of elongate crystals growing towardsthe shell surface (Fig. 5D,E) that is, away from a substratethat is no longer obvious but may have been a mucus sheet(see below). Individual crystals have blunt terminationsand are aragonitic. Sediment grains are cemented into theouter (facing away from the shell surface) surface of thesespherulitic sheets.

The growing shell margins of an air-dried specimen ofSamarangia shows thin mucoid sheets (1±2 mm thick)overlying and partially embedded in the arenaceous layerapparently growing beneath the sheets. Crystals with avariety of morphologies are contained within andprojecting from these mucoid sheets (Fig. 6A-F). In someareas they appear to be growing within the sheets, whileelsewhere, they are apparently growing beneath or areoverlain by mucus.

1) They may be isolated hexagonal crystals 3±4 mm longwhich taper at either end to give a `rice-grain' form(Fig. 6A, D). These sometimes carry subsidiary growthpinnacles so that their terminations are roughened,dividing to form a minutely pinnacled surface, thatresembles surfaces described by Folk et al. (1985; fig. 9).These crystals are about 20 mm long with a length to widthratio of approximately 4 : 1 (Fig. 6D). In some areaspinnacles become increasingly well defined so that thecrystals take on the appearance of bundles of parallel sub-crystals; 2) With these, and randomly arranged on grainsurfaces, are crystal units of generally similar form butconsisting of laterally linked bundles of subcrystals, in-equalities in length producing ragged ends. These are 5±25 mm long with a length to width ratio of approximately3 : 1 (Fig. 6C, E). Groups of similar crystals radiatingfrom a common nucleus (Fig. 6F) form radial clusters asgrowth fills the gaps between divergent axes; 3) grainsurfaces at a distance from the margin are coated with

closely packed elongate (fibrous) crystals with blunt ends,while the sheets of cement consist entirely of such crystals(Fig. 5D,E).

Crystals and mucus on the mantle margin of Granicorium

Critical-point dried preparations of the mantle margin of G.indutum show that the outer surfaces of both the middle andlarger inner fold (imf1) are coated in mucus, and a mucusmass is also present in the space between imf1 and themiddle fold. This material appears to emanate from the boththe outer face of the inner fold and the outer middle foldand in one preparation (Fig. 7A-B) forms a continuousmass extended to the outer surface of the middle fold. Thismucoid material contains abundant rod shaped bacteria andfilaments (Fig. 7C) and can be seen adhering to the outersurface of the periostracum (Fig. 7D). Small, single crystals,and crystal aggregates are present within this mucus mass(Fig. 7E) and bacteria are often closely associated with thegrowing crystals. Crystals within the mucus are commonlyhexagonal prisms which are approximately 2 mm long with alength to width ratio ranging from 1 : 1 mp to more than5 : 1 and with apparently smooth surfaces while others aretabular discs 2±3 mm in diameter with a length to widthratio of about 1 : 3 (Fig. 7D,E). The latter carry minuteprojections on their surfaces, and commonly haveprominent screw dislocations on their terminal faces(Fig. 7E) but both forms occur as isolated crystals or asloose aggregates. Microprobe trace element analysis of thesecrystals suggests that most are calcium carbonate but someare gypsum. The significance of the latter is unclear, theymay be artefactual, but the our observations show that crys-tallization is widespread within the mucus coating themiddle mantle fold.

Discussion

How do Granicorium and Samarangia stick the sand to theshell?

We have no direct observations of the process of sandaccretion. However, the nature and distribution of thecement, the surface of the newly accreted sand grains andthe structures at the mantle edge enable us to propose apossible mechanism.

The bulk of the cements described from Granicoriumand Samarangia resemble marine cements, which are

Fig. 4ÐGranicorium indutum, details of arenaceous layer andcement. ÐA, radial section of shell edge showing encrustingsand layer. Polarized light. Scale bar: 300 mm. ÐB, detail ofquartz grains (Q) encrusted by aragonitic cement. Polarizedlight. Scale bar: 80 mm. ÐC, SEM of fractured section ofarenaceous layer showing aragonitic cement encrusting quartzgrains. Scale bar: 75 mm. ÐD, SEM detail of aragonitic

cement crystals encrusting quartz grain (top left). Scale bar:6 mm. ÐE, SEM of surface of arenaceous layer at shellmargin showing mucus sheet with aragonitic crystals of ricegrain morphology. Scale bar: 7.5 mm. ÐF, surface ofarenaceous layer at shell margin showing mucus sheet withunderlying crystals and bacteria in mucus sheet (arrow). Scalebar: 5 mm.



Fig. 5ÐSamarangia quadrangularis. ÐA, radial section of shell(lower left) and arenaceous layer showing spherulitic sheetsgrowing from the shell surface. Polarized light. Scale bar:250 mm. ÐB, radial section showing successive, truncatedcement sheets (arrow) arising from the shell surface. Shell atbottom, arenaceous layer to top. Scale bar: 100 mm. ÐC, SEMof transverse section through spherulitic sheet (ss) forming a

prominent rib. Scale bar: 500 mm. ÐD, SEM of fracturedsection of spherulitic sheet. Scale bar: 20 mm. ÐE, detail of D.showing radiating groups of needle-like aragonitic crystals. Scalebar: 10 mm. ÐF, SEM of group of aragonitic cement crystalson sediment grain surface. Scale bar: 5 mm. ÐG, SEM ofcement crystals growing in spaces in skeletal sediment grain.Scale bar: 20 mm.

Fig. 6ÐSamarangia quadrangularis, crystal growth at shell margin.All SEMs. ÐA, aragonitic `rice-grain' crystals growing within andbeneath successive mucus sheets (upper peeled back). Scale bar:50 mm. ÐB, sediment grains encrusted by cement crystals andmucus sheets. Scale bar: 200 mm. ÐC, aragonite crystals growing

through and on mucus sheet. Scale bar: 20 mm. ÐD, two phasesof aragonite crystals growing through mucus sheet. Scale bar:20 mm. ÐE, wheat-sheaf crystals growing on cement surface.Scale bar: 20 mm. ÐF, groups of radiating crystals growing onand between sediment grains. Scale bar: 20 mm.



normally viewed as resulting from inorganic processes(Schroeder 1972). However, the cementation process inthese bivalves is clearly under the control of the animaland our evidence suggests that the mucus sheets, seencoating the sand grains at the shell margins of bothGranicorium and Samarangia play an important part in theprocess. The mucus in Granicorium (there were no obser-vations of mantle edges of Samarangia) contains a rich anddiverse microbiota that may also contribute to itsformation. The mucus at the shell margin serves twopurposes; initially it sticks the grains to the shell surfaceand provides structural stability but it also generates anenvironment in which carbonate crystals are able tonucleate and grow.

In both genera described here, the volume of mucusdecreases at a distance from the shell margin, and there isinitially a concomitant increase in the volume of carbonatecement coating the sediment grains. This cement is mor-phologically distinct from the crystals more intimatelyassociated with the biofilm and is characterized by acicular

crystals locally forming crusts and closely packed radiatingclusters and botryoids, morphologically identical to`marine cements' figured from Recent and Holocenecarbonates (Schroeder 1972; Lighty 1985). The distribu-tion of these cements is important. They are thicker andmore consistently distributed on surfaces facing towardsthe ventral margin of the shell. Towards the umbones thevolume of adherent sand decreases and the coatingbecomes thinner. This implies that although the cementthickness increases away from the aperture it does notthicken indefinitely. Thus, a short distance from theaperture, no further cement is formed.

A key feature of the mucus at the mantle margin ofGranicorium is the presence of bacteria which may have animportant role in the calcification process. Microorganismsand the mucus biofilms they generate have beenimplicated in the precipitation of carbonates in a widerange of marine to subaerial environments such assediments, stromatolites, tufas and even hot springs(Friedman et al. 1973; Bauld 1984; Merz 1992; Pedley

Fig. 7ÐMantle margin of Granicorium indutum, critical point driedpreparations. ÐA, radial section through mantle margin showingmantle folds and mucus. if1, inner mantle fold 1; m, mucus; mf,middle mantle fold; of, outer mantle fold. Scale bar: 200 mm. ÐB,outer and middle mantle folds showing middle fold coated with

mucus. Scale bar: 50 mm. ÐC, surface of middle mantle fold coatedin bacteria and mucus. Scale bar: 10 mm. ÐD, outer periostracumsurface with platy crystals associated with bacteria. Scale bar: 5 mm.ÐE, mucus mass on outer surface of middle mantle fold showingcrystals growing on filaments. Scale bar: 2 mm.



1994; Verrecchia et al. 1995; Braithwaite and Zedef 1996;DeÂfarge et al. 1996). A process whereby carbonate is preci-pitated within the polysaccharide sheaths of cyanobacterialcells was described by Verrecchia et al. (1995). However,essentially the same reactions may occur where there is nothick sheath, with diffusion to the outer medium allowingcrystallization outside bacterial structures (Thompson andFerris 1990). We can infer from this that similar reactionscan take place on or within proteinaceous microbialbiofilms. The molecules of microbial sheaths and biofilmsmay bind calcium (Pentecost and Riding 1986) in amanner similar to that suggested in bivalve shell minerali-zation, but we do not see a formal arrangement of thegrowing crystals which implies epitaxy. Perhaps the lastpoint in this analysis is that Verrecchia et al. (1995)describe spherulites which nucleate and grow within themucilage sheath of cyanobacteria and are subsequentlyexpelled into the medium.

In Samarangia, mucus sheets are secreted at intervalsby the bivalve and crystal growth is initiated on andwithin them. The sheets form essentially enclosed cells,trapping fluid (seawater) against the original shell surface

and providing relative isolation from the seawater body.These secretion events are not accompanied by equalsuccess and growth of a number of these cement coatsfails before it finally extends significantly from the shellsurface. As in Granicorium the asymmetry of cement dis-tribution implies an anisotropy in the natant fluid,reasonably explained as a response to flow. However, ifmucus and cement sheets do indeed enclose and isolatewater against the shell surface we might expect aprogressive depletion in both calcium and carbonate inresponse to crystal growth and effectively stagnantconditions in which there would be no net flow andtherefore no asymmetry in the cement forming. Thus, itseems likely that cement growth is entirely dependent onthe presence of the mucus film. Only surfaces accessibleto the mantle margin and coated by such films are able togrow a cement. Growth seems to cease after some intervalbut may be reinitiated if the cement surface is reactivatedwith mucus, generating multilaminar cement crusts.

In summary, we suggest that the cementation proceedsas follows. Granicorium has large and muscular middle andinner mantle folds which can extend beyond the shellmargin and are endowed with extensive subepithelial glandcells (Fig. 8A). These mantle folds produce largequantities of mucus which coats the periostracum andsediment immediately surrounding the shell margin. Theextended mantle may press sand grains against the shelland existing sand layer. The mucus coating on the sandgrains contains an abundant bacterial microbiota whichmodifies the chemical environment so that nucleation andgrowth of calcium carbonate crystals occurs on and withinthe mucus and on the mucus-covered surfaces of sedimentgrains. Once initiated, crystal growth continues until thegrains are firmly locked together. Repeated smearing ofmucus by the mantle continues the cementation process.

The situation in Samarangia is rather more complex,requiring the periodic formation of sheets of spheruliticcrystal growths as well as the cementation of sedimentgrains (Fig. 8B). Because of lack of suitable preservedmaterial, we have no evidence for bacterial involvementbut mucus sheets are certainly implicated. The process ofcementation of sediment grains is essentially similar to thatof Granicorium and probably involves mucus coating of thegrains. We propose that the thicker spherulitic sheets areformed by periodic but regular secretion of thicker, moreextensive, mucus layers. Extensive nucleation and crystalgrowth on and within this mucus layer results in acontinuous sheet of fused spherulites that remains after themucus has decomposed. The formation of the ribsrequires that at these points on the shell margin the mantleextends further and the mucus layers are more extensivethan on other parts of the shell. This process is analogousto the formation of ribs and spines in the primary shell ofbivalves where localized portions of the mantle mustextend periodically to the tips of these structures.

Fig. 8ÐSchematic diagram of radial sections of shell margins ofÐA, Granicorium indutum and ÐB, Samarangia quadrangularisillustrating proposed mechanism of sediment accretion (see textfor details).



The function of the arenaceous layers

We have no direct or experimental evidence for thefunction of the arenaceous layers of Granicorium andSamarangia but some hypotheses are reviewed below.These hypotheses divide into two main categories: thoseconcerned with the properties of the sand layer in resistingvarious types of predation and those concerned withresistance to physical and mechanical stresses.

Predation resistance. Two factors resulting from thearenaceous layer seem important, namely the contributionit makes to the increased total globosity of the animal andto the increased shell thickness. The sand layer increasesthe effective diameter of the animal, a factor which maydeter some manipulative predators such as crabs and fishin which there is a maximum size limit on the prey whichcan be handled by chelae and jaws. Also, for otherpredators such naticid and muricid gastropods whichmanipulate the prey in the foot prior to shell drilling, thereis normally a maximum size of prey that any particularsized predator can handle (Hughes and Dunkin 1984).Thus, the extra diameter of the shell may result in a refugefrom some types of predators.

The sand layers more than double the effective shellthickness particularly near the shell margins. Thicknessalone will give extra strength in resisting crushingpredators. However, the juxtaposition of layers withdifferent mechanical properties may also be a predationresistant strategy. The boundaries between layers ofdifferent microtextures are known to be effective in thedissipation of cracks (Currey 1990). Additionally, apredatory attack may result merely in the flaking off of theouter sand layer, allowing escape. One of the mostvulnerable areas of the bivalved shell is at the junction ofthe valves and some predatory gastropods and Crustaceacause chipping damage at the shell margins of bivalves togain access to their prey (Vermeij 1983). Thickening of theshell margin by sand layers should help resist this type ofpredation.

Resistance to shell drilling by predatory gastropodswhich use both mechanical and chemical means to drillholes (Carriker 1981; Kabat 1990) is a further possibilityfor the function of the arenaceous layers. The presence ofhard quartz grains may confer mechanical resistance toradular scraping, although the acids and chelating agentssecreted by the accessory boring organ would dissolve thecement coatings. Thick shells are known to be moreresistant to attacks by drilling gastropods, with thefrequency of incomplete shell borings being greater onthick shelled species (Vermeij 1987). None of the Rottnestsamples of Granicorium, neither live nor dead shells, showany evidence of drilling. However, some shells in a sampleof Granicorium from 82 m in the Great Australian Bight(Australian Museum AM. C.101916) were drilled. Out of10 disarticulated valves, three had complete drill holes and

another had an incomplete drill hole which penetrated thesand layer as far as the true shell. Additionally, threeincomplete drill holes were found in the bare umbones ofother valves. In another sample, of two whole shells and11 single valves from Frazer Island, Queensland (AMC.121015), one individual had an incomplete drill hole.These drill holes are straight-sided, without a countersunkrim, suggesting a predator from the family Muricidaerather than Naticidae. Amongst the seven individuals ofSamarangia we studied from various localities, only onehad been drilled (Fig. 1F). From this evidence it is clearthat the sand layer does not prevent drilling predation.Nevertheless, the length of time expended in drilling boththe sand layer as well as the true shell may inhibit all butthe most persistent predators.

Finally, the sand layer could act as a camouflage to theshell to confuse visual predators such as fish. However,under normal circumstances Granicorium and Samarangiashould be shallowly buried in the sand substrate. Anotherpossibility is that the sand layers would confuse predatorsthat recognize their prey by touch such as somegastropods.

Resistance to environmental stresses. The sand layersincrease both the weight and tumidity of the animal. Thesefeatures are advantageous for shallow burrowing bivalves,enhancing their stability and resistance to scour in mobilesand substrates (Stanley 1970, 1975). The coarse sandlayer and ribs also gives a rough surface texture to theanimal which may improve anchorage in the sediment, theshell itself being smooth and glossy. The outer layer ofsand could also be an adaptation for resisting shellabrasion due to burrowing or other mechanical wear.

The sand layer may deter the settlement of shell-encrusting epibionts as well as shell borers such as clionidsponges, bryozoans, acrothoracian barnacles, polychaetes,cyanobacteria, or fungi. Evidence that encrustations onshells do indeed discourage shell borers comes from astudy by Smyth (1989), who showed that coral reefgastropods encrusted with a thick coating of coralline algaeare much less susceptible to shell boring organisms. Thisraises the possibility that gastropods somehow selectivelyencourage the coralline algal coating. Our thin sections ofboth Samarangia and Granicorium show that neither theshell nor the sand layer is bored and the outer surfaces ofthe living animals are free of epibionts.

Sand accretion and other extraperiostracal encrustations inother bivalves

Although species from a number of different bivalvefamilies are known to have shells with intra-and extraper-iostracal calcification and encrustations, these differ instructure and mode of formation and are not homologousin the different taxa. Spines, needles and granules, usually



of aragonite but sometimes calcium phosphate, partially orwholly embedded within the periostracum are known inspecies of Mytiloidea, Veneroidea and the subclass Anom-alodesmata (Carter and Aller 1975; Carter 1990; Ohno1996). These are formed by the outer part of the middlemantle fold or the inner part of the outer fold and thecalcified structures are incorporated into the periostracumas it is secreted. Other bivalves have calcareous encrusta-tions which coat part of the shell or modify the shellmargins, as in the case of some species of Lithophaginae.For instance the posterior extensions or `forceps' ofLithophaga aristata are extraperiostracal calcifiedextensions to the posterior part of the shell, believed to beformed by secretions from posterior pallial glands (Morton1993). Some bivalves have calcified tubes which partiallyor totally enclose the animal as in Brechites, Fistulana,Cucurbitula (Morton 1983, 1984, 1985). These are formedfrom secretions from pallial glands around the mantlemargin or around the siphons.

Sand coatings to the shell are less common amongstbivalves and restricted to some Anomalodesmata and theVeneroidea. Thin extraneous sand coatings in species ofLyonsia which adhere to a mucoid layer secreted over athin periostracum are described by Prezant (1981a) whostates p. 295: `This extra coat serves the mollusc inprotecting the shell, stabilizing the bivalve in shiftingsediments by increasing surface area and adding weight tothe shell, and acting as camouflage'. The sand encrusta-tions of lyonsiids are formed in a different way from thoseof Granicorium & Samarangia. Prezant (1981b)) andMorton (1987) show that in lyonsiids there are a series ofdiscrete glands arranged around the mantle margin on theouter surface of the middle mantle fold which secrete aglue which binds sand grains to the outside of the perios-tracum. Similar mantle glands are found in the Verticordii-dae and most species have a thin layer of adheringsediment (Allen and Turner 1974; fig. 37b). However, thesand layer of lyonsiids is rather loosely attached and grainscan be dislodged with a needle. Harper (1997, fig. 4D)shows an SEM phototograph of the periostracum ofLyonsia norvegica with sand grains attached to the outersurface by organic fibres. There is no evidence of acalcified cement. Lyonsiids typically have very thin shellsand the sand coat layer may again provide added thicknessand strength.

Sand encrustations have been observed in some speciesof the veneroidean subfamily Pitarinae (Oliver 1995) and itseemed a possibility that these layers may be similar orhomologous with the encrustations in Granicorium andSamarangia. We have examined such layers in Pitar affinisand P. obliquata from east Africa. In both of these the en-crustation lies around the margin of the shell but isthickest at the posterior. The encrustation is complex andconsists of two distinct layers. Immediately overlaying theperiostracum there is a white calcified layer consisting of

closely packed calcareous needles as is seen in some othervenerids (Ohno 1996). On top of this there is a yellowish,soft organic layer into which sand grains are embedded.The sand grains are not cemented to each other and inalcohol-preserved specimens the layer is soft to the touchof a probe. In other venerids the calcified needles are seenembedded into the periostracum at the proximal ends andare formed simultaneously with the outermost layer of theperiostracum. Apart from the paper by Ohno (1996) andsome unpublished observations of our own, very littleknown about the formation of these extraperiostracalcalcified structures in the Veneridae. However, they areonly known to occur in species of the subfamilies Pitarinaeand Circinae. The distribution needs further study as, likeother encrustations, these are often routinely cleaned frommuseum specimens. Certainly these encrustations differconsiderably from the rigid, highly cemented encrustationsof Samarangia and Granicorium. The calcified granules,spicules and spines in the periostracum of anomalodesma-tan bivalves have been better studied (Aller 1974; Carterand Aller 1975).

Morton (1995) describes the formation of a hard `castle'of agglutinated sand in which Cooperella subdiaphana(Carpenter), a veneroidean bivalve of the family Petricoli-dae from California, is sometimes encased. This is notcemented or attached to the shell and Morton (1995)suggests that it is constructed by the binding of sedimentas a result of outpourings of a secretion from pallial glandscomprising subepithelial cells located in the middle mantlefolds around the pedal gape. Unfortunately, no details aregiven of the agglutinated sand casing or the nature of itscement. It is therefore not known whether the sand is heldtogether by a mineralized cement.

Species of the lucinoidean subgenus Thyasira(Mendicula), for example T. (M.) ferruginea (Locard1886), are characterized by a hard ferruginous outer layerencrusting the periostracum (Payne and Allen 1991). Themineralogy, structure and mode of formation of this layerare unknown. Nevertheless, the occurrence in a restrictedgroup of thyasirids suggests that the formation may becontrolled by the animal rather than an inorganic encrusta-tion.

Finally, shells with arenaceous outer coatings are alsoknown in a few gastropods. These include Scaliola (Bandeland El-Nakhal 1993; Ponder 1994), and the Miocene-Pliocene fossil genera Springvaleia (Turritellidae) andPsammodulus (Modulidae) (J. Todd Pers. Comm.). Addi-tionally, Xenophora spp. cement large sediment pieces ordead shells and corals to their shells (Ponder 1983). Noneof these gastropods have such a thick and continuous sandcoating as Granicorium or Samarangia. Unfortunately,there are no details of the cement or cementing processavailable for these taxa other than the observation byPonder (1994) that the sand grains (quartz) of Scaliolacontinue to adhere to the periostracum after decalcification



of the shell. This suggests that the sediment is attached byan organic adhesive and not by a calcareous cement as inGranicorium and Samarangia.

Conclusions

The encrusting arenaceous layer of Granicorium andSamarangia is an unusual constructional feature ofbivalves. The sand grains are bound to the shell by acement that appears remarkably similar to inorganicmarine cements seen in early sea-floor cementation(Shinn 1969) or in some beachrocks. Evidence suggeststhe primary role of mucus secretions and the possible roleof bacteria in the formation of the cement. The role ofmicrobial films in the formation of calcareous deposits isbeing increasingly recognized in aquatic environmentsand it is possible that the two bivalves are utilizing similarcalcification mechanism to cement sand to their shells.The functional significance of the arenaceous layer isunknown, but resistance to predators and epi-andendobionts are likely factors. The arenaceous layer is oneof a plethora of extraperiostracal calcified structuresfound amongst bivalves and adds to the diversity of calci-fication strategies within the class. The functional signifi-cance of these structures is largely uninvestigated as istheir significance and potential as phylogeneticcharacters. Extraperiostracal structures are oftenperceived as inorganic encrustations and routinelycleaned off shells which has hindered the recognition oftheir biological importance.

Taxonomic note

At present Granicorium and Samarangia are classified intwo different subfamilies of Veneroidea (Keen 1969;Fischer-Piette and Vugadinovic 1977), respectively, theTapetinae and the monospecific Samaranginae. Recently,Harte (1998 p. 360) has suggested that the two generashould be placed together in the Samaranginae. We agreewith this suggestion for similarities of shell morphology(Fig. 1A-H) Ð hinge teeth (3 cardinal teeth in each valve,middle cardinal curved, lateral teeth absent (the smallpustular structure anterior to the anterior cardinal on theleft valve Samarangia may or may not be a vestigial lateraltooth)), lack of pallial sinus, microstructure of shell layers,coupled with the common facility of cementing sedimentto the shell, suggest that the two genera are closely related.This character set is not shared with any other veneroideansubfamily and pending taxonomic revision of the wholesuperfamily the two genera should be placed in thesubfamily Samaranginae.

Apart from Granicorium indutum Hedley 1906 the onlyother described species of Granicorium is G. attonitumIredale 1936 from 82 m off Shoalhaven Bight, New South

Wales. We examined the syntypes of this species(Australian Museum C060638, C306370) and consider ita junior synonym of G. indutum (syntypes AM C18868)However, specimens of Granicorium we have examinedfrom coastal Queensland (for example a sample of 27shells from 19 to 28 m taken 2 km off Tugun Beach, GoldCoast, south of Brisbane in collections of Museum & ArtGallery of the Northern Territory) are larger and lessglobose than either the type material of G. indutum or ourRottnest sample. These may possibly be a separate species.

Acknowledgements

We are grateful to Fred Wells and Di Walker fororganizing the Marine Biological Workshop on RottnestIsland where we initially dredged the Granicorium. IanLoch (Australian Museum), Richard Willan (Art Galleryand Museum of Northern Territory, Darwin) and PhilippeBouchet (MuseÂum National d'Histoire Naturelle, Paris)kindly allowed us access to their collections and loan ofspecimens. Additionally, Philippe Bouchet allowed us tosection a specimen of Samarangia.

We would also like to thank Chris Jones and Alex Ball(Electron Microscope Unit, NHM) for much help andTony Wighton for making the geological thin sections,Dave Cooper for sections of mantle margins and HarryTaylor for macrophotography. Additionally, Brian Morton,Liz Harper and Jon Todd are thanked for usefuldiscussion and helpful suggestions.

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bivalves with 'concrete overcoats': granicorium and samarangia

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